Effects of Wolbachia on genetic divergence between populations: Mainland-island model

Integrative and Comparative Biology, Apr 2002 by Telschow, Arndt, Hammerstein, Peter, Werren, John H

Effects of Wolbachia on Genetic Divergence Between Populations: Mainland-Island Model'

SYNOPSIS. Cytoplasmic incompatibility (CI) induced by intracellular bacteria is a possible mechanism for speciation. Growing empirical evidence suggests that bacteria of the group Wolbachia may indeed act as isolating factors in recent insect speciation. Wolbachia are cytoplasmically transmitted and can cause unior bidirectional CI. We present a mainland-island model to investigate how much impact Wolbachia can have on genetic divergence between populations. In the first scenario we assume that the island population has diverged at a selected locus and ask whether genetic divergence will be maintained after introduction of migration from the mainland. In the second we explore whether divergence will originate under migration. For simplicity, the host organisms are modeled as haploid sexuals. Simulations show that if each population is initially infected with a different strain of Wolbachia, then higher levels of divergence occur at the locally selected locus than in the absence of Wolbachia. A weaker effect is seen when there is only unidirectional CI caused by a single strain of Wolbachia on the island. CI increases divergence because it reduces effective migration between mainland and island. Migrants suffer from being confronted with the wrong CI system and this also applies to their matrilineal descendants. Moreover, there is a strong linkage disequilibrium between host genotype and infection state, which helps to maintain Wolbachia differences between the populations in the face of migration A sex bias in migration can either increase or decrease the effect of Wolbachia on divergence. Results support the view that Wolbachia has the potential for increasing divergence between populations and thus could enhance probabilities of speciation.

INTRODUCTION

Wolbachia are widespread cytoplasmically inherited bacteria, found in approximately 20% of insects (Werren and Windsor, 2000), and also commonly in isopods (Bouchon et al., 1998), mites (Breeuwer, 1997) and nematodes (Bandi et al., 1998). These bacteria cause a number of reproductive alterations in their hosts, including induction of parthenogenesis, feminization of genetic males, male-killing, and cytoplasmic incompatibility (for reviews of Wolbachia see Werren, 1997; Stouthamer et al., 1999). Wolbachia are predominantly inherited through the egg cytoplasm, but not via sperm. As a result, transmission is maternal, and the induced reproductive alterations are generally advantageous to the bacteria because they either increase the fitness or proportion of the transmitting (female) sex (Werren and O'Neill, 1997).

Cytoplasmic incompatibility (CI) is an incompatibility between the sperm and egg (see Hoffman and Turelli, 1997 for a review). Cytologically, the paternal chromosomes condense improperly during the first and subsequent mitoses (O'Neill and Karr, 1990; Breeuwer and Werren, 1990; Reed and Werren, 1995), which typically results in death of the developing zygote. There are two basic forms of CI. Unidirectional CI occurs when males from an "infected" population mate with females from an "uninfected" population. Bidirectional incompatibility can occur when two populations are infected with different strains of Wolbachia. CI can be interpreted as a "modification-rescue" system (Werren, 1997). The bacteria modify the sperm, and the same (or similar) strain of bacteria must be present in the egg to rescue the modification. The modification-rescue model can explain the basic patterns of CI (Fig. 1). Unidirectional incompatibility occurs when the sperm is modified but bacteria are not present in the egg to rescue the modification, whereas the reciprocal cross (uninfected male X infected female) is compatible. Bidirectional incompatibility presumably occurs when different strains of Wolbachia have different modification-rescue systems. However, the biochemical mechanisms of CI remain unknown.

Cytoplasmic incompatibility has attracted attention as a possible mechanism for rapid speciation (Laven, 1959, 1967; Powell, 1982; Werren, 1998; Hurst and Schilthuizen, 1998; Bordenstein et al., 2001). The basic idea is that CI may sufficiently prevent or reduce gene flow between populations to permit divergence and eventual speciation. The discovery that CI is caused by a widespread group of bacteria (Wolbachia) has revitalized interest in its potential role in speciation. However, this idea is controversial (Hurst and Schilthuizen, 1998; Wade, 2001). Empirical studies are accumulating that are consistent with a possible role of Wolbachia in speciation, including evidence that Wolbachia is a major isolating mechanism in some recent speciation events (Breeuwer and Werren, 1990; Shoemaker et al., 1999; Bordenstein et al., 2001), and growing evidence that many insect species harbor different strains of Wolbachia, often in different geographic populations (Mercot et al., 1995).

Surprisingly, there have been virtually no theoretical investigations of the effect of Wolbachia on genetic divergence between populations. Here we investigate this topic, and specifically explore the interactions between migration, selection and Wolbachia induced CI using a mainland-island model. Our results show that Wolbachia induced CI (both unidirectional and bidirectional) can have significant effects on the level of divergence at a selected locus between populations and over a wide range of parameters. A crucial point is that Wolbachia induced CT reduces the effective migration rate between the populations.